Limits...
Polyandry in the medfly - shifts in paternity mediated by sperm stratification and mixing.

Scolari F, Yuval B, Gomulski LM, Schetelig MF, Gabrieli P, Bassetti F, Wimmer EA, Malacrida AR, Gasperi G - BMC Genet. (2014)

Bottom Line: In the Mediterranean fruit fly (medfly), Ceratitis capitata, a highly invasive agricultural pest species, polyandry, associated with sperm precedence, is a recurrent behaviour in the wild.The accumulation of sperm from different males will increase the overall genetic variability of the offspring and will ultimately affect the effective population size.Indeed, even if the female's last mate is sterile, an increasing proportion of sperm from a previous mating with a fertile male may contribute to sire viable progeny.

View Article: PubMed Central - HTML - PubMed

ABSTRACT

Background: In the Mediterranean fruit fly (medfly), Ceratitis capitata, a highly invasive agricultural pest species, polyandry, associated with sperm precedence, is a recurrent behaviour in the wild. The absence of tools for the unambiguous discrimination between competing sperm from different males in the complex female reproductive tract has strongly limited the understanding of mechanisms controlling sperm dynamics and use.

Results: Here we use transgenic medfly lines expressing green or red fluorescent proteins in the spermatozoa, which can be easily observed and unambiguously differentiated within the female fertilization chamber. In twice-mated females, one day after the second mating, sperm from the first male appeared to be homogenously distributed all over the distal portion of each alveolus within the fertilization chamber, whereas sperm from the second male were clearly concentrated in the central portion of each alveolus. This distinct stratified sperm distribution was not maintained over time, as green and red sperm appeared homogeneously mixed seven days after the second mating. This dynamic sperm storage pattern is mirrored by the paternal contribution in the progeny of twice-mated females.

Conclusions: Polyandrous medfly females, unlike Drosophila, conserve sperm from two different mates to fertilize their eggs. From an evolutionary point of view, the storage of sperm in a stratified pattern by medfly females may initially favour the fresher ejaculate from the second male. However, as the second male's sperm gradually becomes depleted, the sperm from the first male becomes increasingly available for fertilization. The accumulation of sperm from different males will increase the overall genetic variability of the offspring and will ultimately affect the effective population size. From an applicative point of view, the dynamics of sperm storage and their temporal use by a polyandrous female may have an impact on the Sterile Insect Technique (SIT). Indeed, even if the female's last mate is sterile, an increasing proportion of sperm from a previous mating with a fertile male may contribute to sire viable progeny.

Show MeSH

Related in: MedlinePlus

Changes in the proportion of offspring sired by the first (P1) and second (P2) male over time from twice-mated females. The mean proportion of progeny sired by 52 wild-type females mated first to tGFP1 males and then to DsRedEx1 males is shown on the left, whereas the mean proportion of progeny sired by 50 females mated according to the reciprocal male order is shown on the right. Green bars represent the progeny attributable to tGFP1, whereas red bars represent the progeny attributable to DsRedEx1 males. Vertical bars indicate standard errors.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4255777&req=5

Figure 1: Changes in the proportion of offspring sired by the first (P1) and second (P2) male over time from twice-mated females. The mean proportion of progeny sired by 52 wild-type females mated first to tGFP1 males and then to DsRedEx1 males is shown on the left, whereas the mean proportion of progeny sired by 50 females mated according to the reciprocal male order is shown on the right. Green bars represent the progeny attributable to tGFP1, whereas red bars represent the progeny attributable to DsRedEx1 males. Vertical bars indicate standard errors.

Mentions: Twice-mated females were also used to obtain a distinct record of paternity for each of the first seven oviposition days (Table 1 and Figure 1). In both reciprocal crosses, the average first male paternity (P1) showed a tendency to increase as more eggs were laid, from 31% on the first day, up to 42% on the seventh oviposition day when tGFP1 males were the first mate, and from 16% to 43% when DsRedEx1 males acted as first mate. To determine whether this apparent trend is statistically significant, a logistic regression analysis was performed using a generalized linear model with binomial errors. The overall regression model slope, corresponding to the oviposition day, was significantly different from zero when the DsRedEx1 males acted as first mate (z = 11.87, P < 2e-16), whereas marginally non-significant when the tGFP1 males acted as first mate (z = 1.798, P = 0.0722). Indeed, in the DsRedEx1,tGFP1 remating parental combination, the P1 values in the first two oviposition days were significantly lower than in the following five days (Wilcoxon rank sum test with continuity correction, P = 4.9e-7), whereas no significant difference was detected in the reciprocal cross (P = 0.80).


Polyandry in the medfly - shifts in paternity mediated by sperm stratification and mixing.

Scolari F, Yuval B, Gomulski LM, Schetelig MF, Gabrieli P, Bassetti F, Wimmer EA, Malacrida AR, Gasperi G - BMC Genet. (2014)

Changes in the proportion of offspring sired by the first (P1) and second (P2) male over time from twice-mated females. The mean proportion of progeny sired by 52 wild-type females mated first to tGFP1 males and then to DsRedEx1 males is shown on the left, whereas the mean proportion of progeny sired by 50 females mated according to the reciprocal male order is shown on the right. Green bars represent the progeny attributable to tGFP1, whereas red bars represent the progeny attributable to DsRedEx1 males. Vertical bars indicate standard errors.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4255777&req=5

Figure 1: Changes in the proportion of offspring sired by the first (P1) and second (P2) male over time from twice-mated females. The mean proportion of progeny sired by 52 wild-type females mated first to tGFP1 males and then to DsRedEx1 males is shown on the left, whereas the mean proportion of progeny sired by 50 females mated according to the reciprocal male order is shown on the right. Green bars represent the progeny attributable to tGFP1, whereas red bars represent the progeny attributable to DsRedEx1 males. Vertical bars indicate standard errors.
Mentions: Twice-mated females were also used to obtain a distinct record of paternity for each of the first seven oviposition days (Table 1 and Figure 1). In both reciprocal crosses, the average first male paternity (P1) showed a tendency to increase as more eggs were laid, from 31% on the first day, up to 42% on the seventh oviposition day when tGFP1 males were the first mate, and from 16% to 43% when DsRedEx1 males acted as first mate. To determine whether this apparent trend is statistically significant, a logistic regression analysis was performed using a generalized linear model with binomial errors. The overall regression model slope, corresponding to the oviposition day, was significantly different from zero when the DsRedEx1 males acted as first mate (z = 11.87, P < 2e-16), whereas marginally non-significant when the tGFP1 males acted as first mate (z = 1.798, P = 0.0722). Indeed, in the DsRedEx1,tGFP1 remating parental combination, the P1 values in the first two oviposition days were significantly lower than in the following five days (Wilcoxon rank sum test with continuity correction, P = 4.9e-7), whereas no significant difference was detected in the reciprocal cross (P = 0.80).

Bottom Line: In the Mediterranean fruit fly (medfly), Ceratitis capitata, a highly invasive agricultural pest species, polyandry, associated with sperm precedence, is a recurrent behaviour in the wild.The accumulation of sperm from different males will increase the overall genetic variability of the offspring and will ultimately affect the effective population size.Indeed, even if the female's last mate is sterile, an increasing proportion of sperm from a previous mating with a fertile male may contribute to sire viable progeny.

View Article: PubMed Central - HTML - PubMed

ABSTRACT

Background: In the Mediterranean fruit fly (medfly), Ceratitis capitata, a highly invasive agricultural pest species, polyandry, associated with sperm precedence, is a recurrent behaviour in the wild. The absence of tools for the unambiguous discrimination between competing sperm from different males in the complex female reproductive tract has strongly limited the understanding of mechanisms controlling sperm dynamics and use.

Results: Here we use transgenic medfly lines expressing green or red fluorescent proteins in the spermatozoa, which can be easily observed and unambiguously differentiated within the female fertilization chamber. In twice-mated females, one day after the second mating, sperm from the first male appeared to be homogenously distributed all over the distal portion of each alveolus within the fertilization chamber, whereas sperm from the second male were clearly concentrated in the central portion of each alveolus. This distinct stratified sperm distribution was not maintained over time, as green and red sperm appeared homogeneously mixed seven days after the second mating. This dynamic sperm storage pattern is mirrored by the paternal contribution in the progeny of twice-mated females.

Conclusions: Polyandrous medfly females, unlike Drosophila, conserve sperm from two different mates to fertilize their eggs. From an evolutionary point of view, the storage of sperm in a stratified pattern by medfly females may initially favour the fresher ejaculate from the second male. However, as the second male's sperm gradually becomes depleted, the sperm from the first male becomes increasingly available for fertilization. The accumulation of sperm from different males will increase the overall genetic variability of the offspring and will ultimately affect the effective population size. From an applicative point of view, the dynamics of sperm storage and their temporal use by a polyandrous female may have an impact on the Sterile Insect Technique (SIT). Indeed, even if the female's last mate is sterile, an increasing proportion of sperm from a previous mating with a fertile male may contribute to sire viable progeny.

Show MeSH
Related in: MedlinePlus